The Influence of Sesquiterpenes from Myrica rubra on the Antiproliferative and Pro-Oxidative Effects of Doxorubicin and Its Accumulation in Cancer Cells

. 2015 Aug 21 ; 20 (8) : 15343-58. [epub] 20150821

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26307963

The sesquiterpenes β-caryophyllene, β-caryophyllene oxide (CAO), α-humulene (HUM), trans-nerolidol (NER), and valencene (VAL) are substantial components of the essential oil from Myrica rubra leaves which has exhibited significant antiproliferative effects in several intestinal cancer cell lines, with CaCo-2 cells being the most sensitive. The present study was designed to evaluate the effects of these sesquiterpenes on the efficacy and toxicity of the anticancer drug doxorubicin (DOX) in CaCo-2 cancer cells and in primary culture of rat hepatocytes. Our results showed that HUM, NER, VAL and CAO inhibited proliferation of CaCo-2 cancer cells but they did not affect the viability of hepatocytes. CAO, NER and VAL synergistically potentiated the efficacy of DOX in cancer cells killing. All sesquiterpenes exhibited the ability to selectively increase DOX accumulation in cancer cells and did not affect DOX concentration in hepatocytes. Additionally, CAO and VAL were able to increase the pro-oxidative effect of DOX in CaCo-2 cells. Moreover, CAO mildly ameliorated DOX toxicity in hepatocytes. Based on all results, CAO seems to be the most promising compound for further testing.

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Merfort I. Perspectives on Sesquiterpene Lactones in Inflammation and Cancer. Curr. Drug Targets. 2011;12:1560–1573. doi: 10.2174/138945011798109437. PubMed DOI

Salminen A., Lehtonen M., Suuronen T., Kaarniranta K., Huuskonen J. Terpenoids: Natural inhibitors of NF-kappa B signaling with anti-inflammatory and anticancer potential. Cell. Mol. Life Sci. 2008;65:2979–2999. doi: 10.1007/s00018-008-8103-5. PubMed DOI PMC

Bartikova H., Hanusova V., Skalova L., Ambroz M., Bousova I. Antioxidant, Pro-Oxidant and Other Biological Activities of Sesquiterpenes. Curr. Top. Med. Chem. 2014;14:2478–2494. doi: 10.2174/1568026614666141203120833. PubMed DOI

Pajak B., Orzechowski A., Gajkowska B. Molecular basis of parthenolide-dependent proapoptotic activity in cancer cells. Folia Histochem. Cytobiol. 2008;46:129–135. doi: 10.2478/v10042-008-0019-2. PubMed DOI

Bhalla Y., Gupta V.K., Jaitak V. Anticancer activity of essential oils: A review. J. Sci. Food Agric. 2013;93:3643–3653. doi: 10.1002/jsfa.6267. PubMed DOI

Huang M., Lu J.J., Huang M.Q., Bao J.L., Chen X.P., Wang Y.T. Terpenoids: Natural products for cancer therapy. Expert Opin. Investig. Drugs. 2012;21:1801–1818. doi: 10.1517/13543784.2012.727395. PubMed DOI

Legault J., Pichette A. Potentiating effect of β-caryophyllene on anticancer activity of α-humulene, isocaryophyllene and paclitaxel. J. Pharm. Pharmacol. 2007;59:1643–1647. doi: 10.1211/jpp.59.12.0005. PubMed DOI

Kim C., Cho S.K., Kim K.D., Nam D., Chung W.S., Jang H.J., Lee S.G., Shim B.S., Sethi G., Ahn K.S. β-Caryophyllene oxide potentiates TNF α-induced apoptosis and inhibits invasion through down-modulation of NF-kappa B-regulated gene products. Apoptosis. 2014;19:708–718. doi: 10.1007/s10495-013-0957-9. PubMed DOI

Abdul A.B., Abdelwahab S.I., Jalinas J.B., Al-Zubairi A.S., Taha M.M.E. Combination of Zerumbone and Cisplatin to Treat Cervical Intraepithelial Neoplasia in Female BALB/c Mice. Int. J. Gynecol. Cancer. 2009;19:1004–1010. doi: 10.1111/IGC.0b013e3181a83b51. PubMed DOI

Xu W.S., Dang Y.Y., Chen X.P., Lu J.J., Wang Y.T. Furanodiene Presents Synergistic Anti-proliferative Activity With Paclitaxel via Altering Cell Cycle and Integrin Signaling in 95-D Lung Cancer Cells. Phytother. Res. 2014;28:296–299. doi: 10.1002/ptr.4984. PubMed DOI

Zhong Z.F., Li Y.B., Wang S.P., Tan W., Chen X.P., Chen M.W., Wang Y.T. Furanodiene enhances tamoxifen-induced growth inhibitory activity of ERa-positive breast cancer cells in a PPAR gamma independent manner. J. Cell. Biochem. 2012;113:2643–2651. doi: 10.1002/jcb.24139. PubMed DOI

Adorjan B., Buchbauer G. Biological properties of essential oils: An updated review. Flavour Fragr. J. 2010;25:407–426. doi: 10.1002/ffj.2024. DOI

Bansal A., Moriarity D.M., Takaku S., Setzer W.N. Chemical composition and cytotoxic activity of the leaf essential oil of Ocotea tonduzii from Monteverde, Costa Rica. Nat. Prod. Commun. 2007;2:781–784.

Erdogan A., Ozkan A. Effects of Thymus revolutus Celak essential oil and its two major components on Hep G2 cells membrane. Biologia. 2013;68:105–111. doi: 10.2478/s11756-012-0144-4. DOI

Raut J.S., Karuppayil S.M. A status review on the medicinal properties of essential oils. Ind. Crops Prod. 2014;62:250–264. doi: 10.1016/j.indcrop.2014.05.055. DOI

Langhansova L., Hanusova V., Rezek J., Stohanslova B., Ambroz M., Kralova V., Vanek T., Lou J.D., Yun Z.L., Yang J., et al. Essential oil from Myrica rubra leaves inhibits cancer cell proliferation and induces apoptosis in several human intestinal lines. Ind. Crops Prod. 2014;59:20–26. doi: 10.1016/j.indcrop.2014.04.018. DOI

Kang W., Li Y., Xu Y., Jiang W., Tao Y. Characterization of Aroma Compounds in Chinese Bayberry (Myrica rubra Sieb. et Zucc.) by Gas Chromatography Mass Spectrometry (GC-MS) and Olfactometry (GC-O) J. Food Sci. 2012;77:C1030–C1035. doi: 10.1111/j.1750-3841.2012.02747.x. PubMed DOI

Hanusova V., Bousova I., Skalova L. Possibilities to increase the effectiveness of doxorubicin in cancer cells killing. Drug Metab. Rev. 2011;43:540–557. doi: 10.3109/03602532.2011.609174. PubMed DOI

Sun C.D., Huang H.Z., Xu C.J., Li X., Chen K.S. Biological Activities of Extracts from Chinese Bayberry (Myrica rubra Sieb. et Zucc.): A Review. Plant Foods Hum. Nutr. 2013;68:97–106. doi: 10.1007/s11130-013-0349-x. PubMed DOI

El Hadri A., del Rio M.A.G., Sanz J., Coloma A.G., Idaomar M., Ozonas B.R., Gonzalez J.B., Reus M.I.S. Cytotoxic activity of α-humulene and trans-caryophyllene from Salvia officinalis in animal and human tumor cells. Anal. Real Acad. Nac. Farm. 2010;76:343–356.

Legault J., Dahl W., Debiton E., Pichette A., Madelmont J.C. Antitumor activity of balsam fir oil: Production of reactive oxygen species induced by α-humulene as possible mechanism of action. Planta Med. 2003;69:402–407. PubMed

Sylvestre M., Pichette A., Lavoie S., Longtin A., Legault J. Composition and cytotoxic activity of the leaf essential oil of Comptonia peregrina (L.) Coulter. Phytother. Res. 2007;21:536–540. doi: 10.1002/ptr.2095. PubMed DOI

Liu K., Chen Q., Liu Y., Zhou X., Wang X. Isolation and Biological Activities of Decanal, Linalool, Valencene, and Octanal from Sweet Orange Oil. J. Food Sci. 2012;77:C1156–C1161. doi: 10.1111/j.1750-3841.2012.02924.x. PubMed DOI

Jun N.J., Mosaddik A., Moon J.Y., Jang K.C., Lee D.S., Ahn K.S., Cho S.K. Cytotoxic Activity of β-Caryophyllene Oxide Isolated from Jeju Guava (Psidium cattleianum Sabine) Leaf. Rec. Natl. Prod. 2011;5:242–246.

Park K.R., Nam D., Yun H.M., Lee S.G., Jang H.J., Sethi G., Cho S.K., Ahn K.S. β-Caryophyllene oxide inhibits growth and induces apoptosis through the suppression of PI3K/AKT/mTOR/S6K1 pathways and ROS-mediated MAPKs activation. Cancer Lett. 2011;312:178–188. doi: 10.1016/j.canlet.2011.08.001. PubMed DOI

Di Sotto A., Maffei F., Hrelia P., Castelli F., Sarpietro M.G., Mazzanti G. Genotoxicity assessment of β-caryophyllene oxide. Regul. Toxicol. Pharmacol. 2013;66:264–268. doi: 10.1016/j.yrtph.2013.04.006. PubMed DOI

Chang H.J., Kim H.J., Chun H.S. Quantitative structure-activity relationship (QSAR) for neuroprotective activity of terpenoids. Life Sci. 2007;80:835–841. doi: 10.1016/j.lfs.2006.11.009. PubMed DOI

Krishnaiah Y.S.R., Al-Saidan S.M., Jayaram B. Effect of nerodilol, carvone and anethole on the in vitro transdermal delivery of selegiline hydrochloride. Pharmazie. 2006;61:46–53. PubMed

Saeedi M., Morteza-Semnani K. Penetration-Enhancing Effect of the Essential Oil and Methanolic Extract of Eryngium bungei on Percutaneous Absorption of Piroxicam through Rat Skin. J. Essent. Oil Bear. Plants. 2009;12:728–741. doi: 10.1080/0972060X.2009.10643782. DOI

Williams A.C., Barry B.W. Penetration enhancers. Adv. Drug Deliv. Rev. 2012;64:128–137. doi: 10.1016/j.addr.2012.09.032. PubMed DOI

Chou T.C. Drug Combination Studies and Their Synergy Quantification Using the Chou-Talalay Method. Cancer Res. 2010;70:440–446. doi: 10.1158/0008-5472.CAN-09-1947. PubMed DOI

Mahmoud S.S., Torchilin V.P. Hormetic/Cytotoxic Effects of Nigella sativa Seed Alcoholic and Aqueous Extracts on MCF-7 Breast Cancer Cells Alone or in Combination with Doxorubicin. Cell Biochem. Biophys. 2013;66:451–460. doi: 10.1007/s12013-012-9493-4. PubMed DOI

Riganti C., Doublier S., Costamagna C., Aldieri E., Pescarmona G., Ghigo D., Bosia A. Activation of nuclear factor-kappa B pathway by Simvastatin and RhoA silencing increases doxorubicin cytotoxicity in human colon cancer HT29 cells. Mol. Pharmacol. 2008;74:476–484. doi: 10.1124/mol.108.045286. PubMed DOI

Wozniak M., Szulawska-Mroczek A., Hartman M.L., Nejc D., Czyz M. Parthenolide Complements the Cell Death-inducing Activity of Doxorubicin in Melanoma Cells. Anticancer Res. 2013;33:3205–3212. PubMed

Martin-Cordero C., Leon-Gonzalez A.J., Calderon-Montano J.M., Burgos-Moron E., Lopez-Lazaro M. Pro-Oxidant Natural Products as Anticancer Agents. Curr. Drug Targets. 2012;13:1006–1028. doi: 10.2174/138945012802009044. PubMed DOI

Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov. 2009;8:579–591. doi: 10.1038/nrd2803. PubMed DOI

Li X., Fang P., Mai J., Choi E.T., Wang H., Yang X.F. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 2013;6:19. doi: 10.1186/1756-8722-6-19. PubMed DOI PMC

Pacifico S., D’Abrosca B., Golino A., Mastellone C., Piccolella S., Fiorentino A., Monaco P. Antioxidant evaluation of polyhydroxylated nerolidols from redroot pigweed (Amaranthus retroflexus) leaves. Lwt-Food Sci. Technol. 2008;41:1665–1671. doi: 10.1016/j.lwt.2007.10.006. DOI

Vinholes J., Goncalves P., Martel F., Coimbra M.A., Rocha S.M. Assessment of the antioxidant and antiproliferative effects of sesquiterpenic compounds in in vitro CaCo-2 cell models. Food Chem. 2014;156:204–211. doi: 10.1016/j.foodchem.2014.01.106. PubMed DOI

Wang H., Joseph J.A. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 1999;27:612–616. doi: 10.1016/S0891-5849(99)00107-0. PubMed DOI

Skarka A., Skarydova L., Stambergova H., Wsol V. Anthracyclines and their metabolism in human liver microsomes and the participation of the new microsomal carbonyl reductase. Chem. Biol. Interact. 2011;191:66–74. doi: 10.1016/j.cbi.2010.12.016. PubMed DOI

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